Prevention of relapse to methamphetamine self-administration by environmental enrichment: involvement of glucocorticoid receptors.
Addiction
Craving
Environmental enrichment
Glucocorticoid receptors
Self-administration
Journal
Psychopharmacology
ISSN: 1432-2072
Titre abrégé: Psychopharmacology (Berl)
Pays: Germany
ID NLM: 7608025
Informations de publication
Date de publication:
Apr 2022
Apr 2022
Historique:
received:
29
10
2020
accepted:
21
01
2021
pubmed:
27
3
2021
medline:
9
4
2022
entrez:
26
3
2021
Statut:
ppublish
Résumé
In rodents, environmental enrichment (EE) produces both preventive and curative effects on drug addiction, and this effect is believed to depend at least in part on EE's actions on the stress system. This study investigated whether exposure to EE during abstinence reduces methamphetamine seeking after extended self-administration. In addition, we investigated whether these effects are associated with alterations in the levels of glucocorticoid receptors (GR) in the brain and whether administration of GR antagonists blocks methamphetamine relapse. We allowed rats to self-administer methamphetamine for twenty 14-h sessions. After 3 weeks of abstinence either in standard (SE) or EE conditions, we measured methamphetamine seeking in a single 3-h session. Then, we used western blot techniques to measure GR levels in several brain areas. Finally, in an independent group of rats, after methamphetamine self-administration and abstinence in SE, we administered the GR antagonist mifepristone, and we investigated methamphetamine seeking. Exposure to EE reduced methamphetamine seeking and reversed methamphetamine-induced increases in GR levels in the ventral and dorsal hippocampus. In addition, EE decreased GR levels in the amygdala in drug-naive animals, but this effect was prevented by previous exposure to methamphetamine. Administration of mifepristone significantly decreased methamphetamine seeking. The anti-craving effects of EE are paralleled by restoration of methamphetamine-induced dysregulation of GR in the hippocampus. These results provide support for the hypothesis that the effect of EE on methamphetamine relapse is at least in part mediated by EE's action on the brain stress system.
Identifiants
pubmed: 33768375
doi: 10.1007/s00213-021-05770-6
pii: 10.1007/s00213-021-05770-6
doi:
Substances chimiques
Receptors, Glucocorticoid
0
Mifepristone
320T6RNW1F
Methamphetamine
44RAL3456C
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1009-1018Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Berger SP, Hall S, Mickalian JD et al (1996) Haloperidol antagonism of cue-elicited cocaine craving. Lancet 347:504–508. https://doi.org/10.1016/s0140-6736(96)91139-3
doi: 10.1016/s0140-6736(96)91139-3
pubmed: 8596268
Blouin AM, Pisupati S, Hoffer CG, Hafenbreidel M, Jamieson SE, Rumbaugh G, Miller CA (2019) Social stress-potentiated methamphetamine seeking. Addict Biol. 24:958–968. https://doi.org/10.1111/adb.12666
doi: 10.1111/adb.12666
pubmed: 30105771
Chauvet C, Lardeux V, Goldberg SR, Jaber M, Solinas M (2009) Environmental enrichment reduces cocaine seeking and reinstatement induced by cues and stress but not by cocaine. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 34:2767–2778. https://doi.org/10.1038/npp.2009.127
doi: 10.1038/npp.2009.127
Courtney KE, Ray LA (2014) Methamphetamine: an update on epidemiology, pharmacology, clinical phenomenology, and treatment literature. Drug Alcohol Depend 143:11–21. https://doi.org/10.1016/j.drugalcdep.2014.08.003
doi: 10.1016/j.drugalcdep.2014.08.003
pubmed: 25176528
Crofton EJ, Zhang Y, Green TA (2015) Inoculation stress hypothesis of environmental enrichment. Neurosci Biobehav Rev 49:19–31. https://doi.org/10.1016/j.neubiorev.2014.11.017
doi: 10.1016/j.neubiorev.2014.11.017
pubmed: 25449533
de Jong IEM, de Kloet ER (2004) Glucocorticoids and vulnerability to psychostimulant drugs: toward substrate and mechanism. Ann N Y Acad Sci 1018:192–198. https://doi.org/10.1196/annals.1296.022
doi: 10.1196/annals.1296.022
pubmed: 15240368
Deroche-Gamonet V, Sillaber I, Aouizerate B, Izawa R, Jaber M, Ghozland S, Kellendonk C, le Moal M, Spanagel R, Schütz G, Tronche F, Piazza PV (2003) The glucocorticoid receptor as a potential target to reduce cocaine abuse. J Neurosci Off J Soc Neurosci 23:4785–4790. https://doi.org/10.1523/JNEUROSCI.23-11-04785.2003
doi: 10.1523/JNEUROSCI.23-11-04785.2003
Enoch M-A (2011) The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology (Berl) 214:17–31. https://doi.org/10.1007/s00213-010-1916-6
doi: 10.1007/s00213-010-1916-6
Ewing S, Ranaldi R (2018) Environmental enrichment facilitates cocaine abstinence in an animal conflict model. Pharmacol Biochem Behav 166:35–41. https://doi.org/10.1016/j.pbb.2018.01.006
doi: 10.1016/j.pbb.2018.01.006
pubmed: 29407873
Farnia V, Farshchian F, Farshchian N, Alikhani M, Sadeghi Bahmani D, Brand S (2020) Comparisons of voxel-based morphometric brain volumes of individuals with methamphetamine-induced psychotic disorder and schizophrenia spectrum disorder and healthy controls. Neuropsychobiology 79:170–178. https://doi.org/10.1159/000504576
doi: 10.1159/000504576
pubmed: 31794972
Fiancette JF, Balado E, Piazza PV, Deroche-Gamonet V (2010) Mifepristone and spironolactone differently alter cocaine intravenous self-administration and cocaine-induced locomotion in C57BL/6 J mice. Addict Biol 15:81–87. https://doi.org/10.1111/j.1369-1600.2009.00178.x
doi: 10.1111/j.1369-1600.2009.00178.x
pubmed: 19799583
Galaj E, Manuszak M, Ranaldi R (2016) Environmental enrichment as a potential intervention for heroin seeking. Drug Alcohol Depend 163:195–201. https://doi.org/10.1016/j.drugalcdep.2016.04.016
doi: 10.1016/j.drugalcdep.2016.04.016
pubmed: 27125660
Galinato MH, Lockner JW, Fannon-Pavlich MJ, Sobieraj JC, Staples MC, Somkuwar SS, Ghofranian A, Chaing S, Navarro AI, Joea A, Luikart BW, Janda KD, Heyser C, Koob GF, Mandyam CD (2018) A synthetic small-molecule Isoxazole-9 protects against methamphetamine relapse. Mol Psychiatry 23:629–638. https://doi.org/10.1038/mp.2017.46
doi: 10.1038/mp.2017.46
pubmed: 28348387
Glynn RM, Rosenkranz JA, Wolf ME, Caccamise A, Shroff F, Smith AB, Loweth JA (2018) Repeated restraint stress exposure during early withdrawal accelerates incubation of cue-induced cocaine craving. Addict Biol 23:80–89. https://doi.org/10.1111/adb.12475
doi: 10.1111/adb.12475
pubmed: 27859963
Goeders NE, Guerin GF (1996) Role of corticosterone in intravenous cocaine self-administration in rats. Neuroendocrinology 64:337–348. https://doi.org/10.1159/000127137
doi: 10.1159/000127137
pubmed: 8930934
Hart EE, Gerson JO, Izquierdo A (2018) Persistent effect of withdrawal from intravenous methamphetamine self-administration on brain activation and behavioral economic indices involving an effort cost. Neuropharmacology 140:130–138. https://doi.org/10.1016/j.neuropharm.2018.07.023
doi: 10.1016/j.neuropharm.2018.07.023
pubmed: 30053443
pmcid: 6442736
Hofford RS, Darna M, Wilmouth CE, Dwoskin LP, Bardo MT (2014) Environmental enrichment reduces methamphetamine cue-induced reinstatement but does not alter methamphetamine reward or VMAT2 function. Behav Brain Res 270:151–158. https://doi.org/10.1016/j.bbr.2014.05.007
doi: 10.1016/j.bbr.2014.05.007
pubmed: 24821405
pmcid: 4096828
Hofford RS, Prendergast MA, Bardo MT (2015) Pharmacological manipulation of glucocorticoid receptors differentially affects cocaine self-administration in environmentally enriched and isolated rats. Behav Brain Res 283:196–202. https://doi.org/10.1016/j.bbr.2015.01.049
doi: 10.1016/j.bbr.2015.01.049
pubmed: 25655510
pmcid: 4351170
Istin M, Thiriet N, Solinas M (2017) Behavioral flexibility predicts increased ability to resist excessive methamphetamine self-administration. Addict Biol. 22(4):958–966. https://doi.org/10.1111/adb.12384
doi: 10.1111/adb.12384
pubmed: 26969296
Joels M, Sarabdjitsingh RA, Karst H (2012) Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol Rev 64:901–938. https://doi.org/10.1124/pr.112.005892
doi: 10.1124/pr.112.005892
pubmed: 23023031
Kabbaj M, Yoshida S, Numachi Y, Matsuoka H, Devine DP, Sato M (2003) Methamphetamine differentially regulates hippocampal glucocorticoid and mineralocorticoid receptor mRNAs in Fischer and Lewis rats. Brain Res Mol Brain Res 117:8–14. https://doi.org/10.1016/s0169-328x(03)00257-2
doi: 10.1016/s0169-328x(03)00257-2
pubmed: 14499476
Kendall JW Jr, Matsuda K, Duyck C, Greer MA (1964) Studies of the Location of the Receptor Site for Negative Feedback Control of Acth Release. Endocrinology 74:279–283. https://doi.org/10.1210/endo-74-2-279
doi: 10.1210/endo-74-2-279
pubmed: 14122535
Kolb B, Gorny G, Li Y, Samaha AN, Robinson TE (2003) Amphetamine or cocaine limits the ability of later experience to promote structural plasticity in the neocortex and nucleus accumbens. Proc Natl Acad Sci U S A 100:10523–10528. https://doi.org/10.1073/pnas.1834271100
doi: 10.1073/pnas.1834271100
pubmed: 12939407
pmcid: 193594
Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 24:97–129. https://doi.org/10.1016/S0893-133X(00)00195-0
doi: 10.1016/S0893-133X(00)00195-0
Koob GF, Le Moal M (2005) Plasticity of reward neurocircuitry and the “dark side” of drug addiction. Nat Neurosci 8:1442–1444. https://doi.org/10.1038/nn1105-1442
doi: 10.1038/nn1105-1442
pubmed: 16251985
Koob GF, Mason BJ (2016) Existing and future drugs for the treatment of the dark side of addiction. Annu Rev Pharmacol Toxicol 56:299–322. https://doi.org/10.1146/annurev-pharmtox-010715-103143
doi: 10.1146/annurev-pharmtox-010715-103143
pubmed: 26514207
Le Moal M, Koob GF (2007) Drug addiction: pathways to the disease and pathophysiological perspectives. Eur Neuropsychopharmacol J Eur Coll Neuropsychopharmacol 17:377–393. https://doi.org/10.1016/j.euroneuro.2006.10.006
doi: 10.1016/j.euroneuro.2006.10.006
Lü X, Zhao C, Zhang L, Ma B, Lou Z, Sun Y, Chen J, Wu W, Beveridge TJR, Zhou W, Liu Y (2012) The effects of rearing condition on methamphetamine self-administration and cue-induced drug seeking. Drug Alcohol Depend 124:288–298. https://doi.org/10.1016/j.drugalcdep.2012.01.022
doi: 10.1016/j.drugalcdep.2012.01.022
pubmed: 22377091
Mantsch JR, Baker DA, Funk D, Lê AD, Shaham Y (2016) Stress-induced reinstatement of drug seeking: 20 years of progress. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 41:335–356. https://doi.org/10.1038/npp.2015.142
doi: 10.1038/npp.2015.142
McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci. 22:105–122. https://doi.org/10.1146/annurev.neuro.22.1.105
doi: 10.1146/annurev.neuro.22.1.105
pubmed: 10202533
McEwen BS (2016) In pursuit of resilience: stress, epigenetics, and brain plasticity. Ann N Y Acad Sci. 1373:56–64. https://doi.org/10.1111/nyas.13020
doi: 10.1111/nyas.13020
pubmed: 26919273
McOmish CE, Hannan AJ (2007) Enviromimetics: exploring gene environment interactions to identify therapeutic targets for brain disorders. Expert Opin Ther Targets 11:899–913. https://doi.org/10.1517/14728222.11.7.899
doi: 10.1517/14728222.11.7.899
pubmed: 17614759
Mifsud KR, Reul JMHM (2018) Mineralocorticoid and glucocorticoid receptor-mediated control of genomic responses to stress in the brain. Stress. 21:389–402. https://doi.org/10.1080/10253890.2018.1456526
doi: 10.1080/10253890.2018.1456526
pubmed: 29614900
Morimasa T, Wirz-Justice A, Kraeuchi K, Arendt J, Baumann J, Haeusler A, Degen P, Feer H (1987) Chronic methamphetamine and its withdrawal modify behavioral and neuroendocrine circadian rhythms. Physiol Behav 39:699–705. https://doi.org/10.1016/0031-9384(87)90253-8
doi: 10.1016/0031-9384(87)90253-8
pubmed: 3602122
Novaes LS, Dos Santos NB, Batalhote RFP et al (2017) Environmental enrichment protects against stress-induced anxiety: Role of glucocorticoid receptor, ERK, and CREB signaling in the basolateral amygdala. Neuropharmacology 113:457–466. https://doi.org/10.1016/j.neuropharm.2016.10.026
doi: 10.1016/j.neuropharm.2016.10.026
pubmed: 27815155
Panlilio LV, Goldberg SR (2007) Self-administration of drugs in animals and humans as a model and an investigative tool. Addict Abingdon Engl 102:1863–1870. https://doi.org/10.1111/j.1360-0443.2007.02011.x
doi: 10.1111/j.1360-0443.2007.02011.x
Papilloud A, Veenit V, Tzanoulinou S, Riccio O, Zanoletti O, Guillot de Suduiraut I, Grosse J, Sandi C (2019) Peripubertal stress-induced heightened aggression: modulation of the glucocorticoid receptor in the central amygdala and normalization by mifepristone treatment. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 44:674–682. https://doi.org/10.1038/s41386-018-0110-0
doi: 10.1038/s41386-018-0110-0
Recinto P, Samant AR, Chavez G, Kim A, Yuan CJ, Soleiman M, Grant Y, Edwards S, Wee S, Koob GF, George O, Mandyam CD (2012) Levels of neural progenitors in the hippocampus predict memory impairment and relapse to drug seeking as a function of excessive methamphetamine self-administration. Neuropsychopharmacology 37:1275–1287. https://doi.org/10.1038/npp.2011.315
doi: 10.1038/npp.2011.315
pubmed: 22205547
Rosenzweig MR, Bennett EL, Hebert M, Morimoto H (1978) Social grouping cannot account for cerebral effects of enriched environments. Brain Res 153:563–576. https://doi.org/10.1016/0006-8993(78)90340-2
doi: 10.1016/0006-8993(78)90340-2
pubmed: 698794
Shaham Y, Shalev U, Lu L, de Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168:3–20. https://doi.org/10.1007/s00213-002-1224-x
doi: 10.1007/s00213-002-1224-x
Shilling PD, Kelsoe JR, Segal DS (1996) Hippocampal glucocorticoid receptor mRNA is up-regulated by acute and down-regulated by chronic amphetamine treatment. Brain Res Mol Brain Res 38:156–160. https://doi.org/10.1016/0169-328x(96)00009-5
doi: 10.1016/0169-328x(96)00009-5
pubmed: 8737679
Shilpa BM, Bhagya V, Harish G, Srinivas Bharath MM, Shankaranarayana Rao BS (2017) Environmental enrichment ameliorates chronic immobilisation stress-induced spatial learning deficits and restores the expression of BDNF, VEGF, GFAP and glucocorticoid receptors. Prog Neuropsychopharmacol Biol Psychiatry 76:88–100. https://doi.org/10.1016/j.pnpbp.2017.02.025
doi: 10.1016/j.pnpbp.2017.02.025
pubmed: 28288856
Sikora M, Nicolas C, Istin M, Jaafari N, Thiriet N, Solinas M (2018) Generalization of effects of environmental enrichment on seeking for different classes of drugs of abuse. Behav Brain Res 341:109–113. https://doi.org/10.1016/j.bbr.2017.12.027
doi: 10.1016/j.bbr.2017.12.027
pubmed: 29288750
Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158:343–359. https://doi.org/10.1007/s002130100917
doi: 10.1007/s002130100917
Sinha R (2008) Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141:105–130. https://doi.org/10.1196/annals.1441.030
doi: 10.1196/annals.1441.030
pubmed: 18991954
pmcid: 2732004
Sinha R, Shaham Y, Heilig M (2011) Translational and reverse translational research on the role of stress in drug craving and relapse. Psychopharmacology (Berl). 218:69–82. https://doi.org/10.1007/s00213-011-2263-y
doi: 10.1007/s00213-011-2263-y
pubmed: 21494792
pmcid: 3192289
Solinas M, Chauvet C, Thiriet N, el Rawas R, Jaber M (2008) Reversal of cocaine addiction by environmental enrichment. Proc Natl Acad Sci U S A 105:17145–17150. https://doi.org/10.1073/pnas.0806889105
doi: 10.1073/pnas.0806889105
pubmed: 18955698
pmcid: 2579392
Solinas M, Thiriet N, Chauvet C, Jaber M (2010) Prevention and treatment of drug addiction by environmental enrichment. Prog Neurobiol 92:572–592. https://doi.org/10.1016/j.pneurobio.2010.08.002
doi: 10.1016/j.pneurobio.2010.08.002
pubmed: 20713127
Solinas M, Chauvet C, Lafay-Chebassier C, Jaafari N, Thiriet N (2020) Environmental enrichment-inspired pharmacological tools for the treatment of addiction. Curr Opin Pharmacol 56:22–28. https://doi.org/10.1016/j.coph.2020.09.001
doi: 10.1016/j.coph.2020.09.001
pubmed: 32966941
Stairs DJ, Prendergast MA, Bardo MT (2011) Environmental-induced differences in corticosterone and glucocorticoid receptor blockade of amphetamine self-administration in rats. Psychopharmacology (Berl) 218:293–301. https://doi.org/10.1007/s00213-011-2448-4
doi: 10.1007/s00213-011-2448-4
Stringfield SJ, Higginbotham JA, Fuchs RA (2016) Requisite Role of Basolateral Amygdala Glucocorticoid Receptor Stimulation in Drug Context-Induced Cocaine-Seeking Behavior. Int J Neuropsychopharmacol 19: https://doi.org/10.1093/ijnp/pyw073
Thiel KJ, Sanabria F, Pentkowski NS, Neisewander JL (2009) Anti-craving effects of environmental enrichment. Int J Neuropsychopharmacol 12:1151–1156. https://doi.org/10.1017/S1461145709990472
doi: 10.1017/S1461145709990472
pubmed: 19691875
Trujillo V, Durando PE, Suarez MM (2016) Maternal separation in early life modifies anxious behavior and Fos and glucocorticoid receptor expression in limbic neurons after chronic stress in rats: effects of tianeptine. Stress 19:91–103. https://doi.org/10.3109/10253890.2015.1105958
doi: 10.3109/10253890.2015.1105958
pubmed: 26452320
Vendruscolo LF, Barbier E, Schlosburg JE, Misra KK, Whitfield TW, Logrip ML, Rivier C, Repunte-Canonigo V, Zorrilla EP, Sanna PP, Heilig M, Koob GF (2012) Corticosteroid-dependent plasticity mediates compulsive alcohol drinking in rats. J Neurosci Off J Soc Neurosci 32:7563–7571. https://doi.org/10.1523/JNEUROSCI.0069-12.2012
doi: 10.1523/JNEUROSCI.0069-12.2012
Williams MT, Inman-Wood SL, Morford LL et al (2000) Preweaning treatment with methamphetamine induces increases in both corticosterone and ACTH in rats. Neurotoxicol Teratol 22:751–759. https://doi.org/10.1016/s0892-0362(00)00091-x
doi: 10.1016/s0892-0362(00)00091-x
pubmed: 11106868
Zhou Y, Proudnikov D, Yuferov V, Kreek MJ (2010) Drug-induced and genetic alterations in stress-responsive systems: implications for specific addictive diseases. Brain Res 1314:235–252. https://doi.org/10.1016/j.brainres.2009.11.015
doi: 10.1016/j.brainres.2009.11.015
pubmed: 19914222
Zuloaga DG, Johnson LA, Agam M, Raber J (2014) Sex differences in activation of the hypothalamic-pituitary-adrenal axis by methamphetamine. J Neurochem 129:495–508. https://doi.org/10.1111/jnc.12651
doi: 10.1111/jnc.12651
pubmed: 24400874
pmcid: 3997586